QUICK SEARCH:   [advanced] Author: Keyword(s): Year:  Vol:  Page:

This Article Abstract Full Text (PDF) Purchase Article View Shopping Cart Alert me when this article is cited Alert me if a correction is posted Services Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Morita, T. Articles by Kiriyama, S. Search for Related Content PubMed PubMed Citation Articles by Morita, T. Articles by Kiriyama, S.

---

Articles

Oligo-L-Methionine and Resistant Protein Promote Cecal Butyrate Production in Rats Fed Resistant Starch and Fructooligosaccharide¹

Azusawa Research Laboratories, Institute for Consumer Healthcare, Yamanouchi Pharmaceutical Company, Itabashi-ku, Tokyo 174-8511, Japan and ^* Laboratory of Nutritional Biochemistry, Otsuma Women's University, Tokyo 102-8357, Japan

²To whom correspondence should be addressed.

	ABSTRACT

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS Feeding studies RESULTS DISCUSSION REFERENCES

 
We examined the role of resistant protein and peptides in promoting cecal butyrate production in rats fed rapidly fermentable carbohydrates. Rats were fed diets containing raw potato starch (RPS, 200 g/kg diet) or fructooligosaccharide (FOS, 60 g/kg diet) with casein, soy or rice protein (250 g/kg diet) for 13 d. In rats fed RPS with casein, the major cecal organic acid was acetate (441 µmol), but lactate and succinate were also found in considerable amounts (324 µmol). Succinate was the major cecal organic acid (235 µmol) in rats fed FOS with casein. When rice protein was fed with RPS, the contribution of lactate was significantly lower and that of propionate tended to be higher (P < 0.1) than in rats fed casein. In rats fed rice protein with FOS, cecal butyrate and acetate were greater and cecal succinate was lower than in rats fed casein with FOS (P < 0.05). Despite the similar amounts of undigested protein in rice and soy proteins, soy protein did not similarly affect cecal butyrate in rats fed FOS or RPS. In another experiment, rats were fed diets containing high amylose cornstarch (HAS, 200 g/kg diet) with casein, casein + oligo-L-methionine (OM, 3 g/kg diet), soy protein, soy protein + OM (3 g/kg diet) or rice protein (250 g/kg diet) for 10 d. OM (digestibility, 31%) was substituted for the same amount of casein. Rats fed rice protein had greater cecal butyrate than rats fed casein (P < 0.05). OM supplementation to casein or soy protein increased cecal butyrate compared with rats fed casein or soy protein alone (P < 0.05). These data support our hypothesis that resistant protein and peptides promote cecal butyrate production and suggest that the differing potency of rice and soy proteins in promoting cecal butyrate production might be explained in part by the different amino acid composition of resistant protein.

KEY WORDS: • fermentable carbohydrate • cecal butyrate • resistant protein • oligo-L-methionine • rats

	INTRODUCTION

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS Feeding studies RESULTS DISCUSSION REFERENCES

 
The relationship between dietary complex carbohydrates and butyrate production in the large bowel microflora has attracted much attention because this short-chain fatty acid (SCFA)³ is an important fuel for colonic epithelial cells (Roediger 1980 ), and in some circumstances, has been shown to inhibit the growth of certain neoplastic cell lines (Candido et al. 1978 , Whitehead et al. 1986 ). Cummings and Macfarlane (1991) concluded from in vitro studies with human fecal inocula that starch was the best substrate of the polysaccharides tested for butyrate production. This was supported by the in vivo findings of Scheppach et al. (1988) that high levels of butyrate were formed in human feeding studies.

However, the evidence from in vitro studies by Macfarlane and Macfarlane (1993) suggested that the end products of bacterial fermentation were influenced by the substrate levels (carbohydrate and nitrogen sources) in the cultures and by the rate at which carbohydrate became available to the bacteria. Our previous studies (Morita et al. 1998 ) clearly demonstrated that the dietary protein source had a substantial influence on the cecal fermentation products of high amylose cornstarch (HAS) because of the different digestibilities of each protein source. This observation suggests that resistant protein and peptides might play an important role in correcting an imbalance in the ratio of carbohydrate to nitrogen as fermentative substrates for cecal bacteria and in promoting n-butyrate production (Morita et al. 1998 ). This hypothesis might be also true for other fermentable carbohydrates that have relatively rapid fermentation rates, e.g., raw potato starch (RPS) and fructooligosaccharide (FOS) (Hidaka et al. 1986 , Hosoya et al. 1988 , Levrat et al. 1991 ).

Further, previous studies (Morita et al. 1998 ) showed that cecal fermentation products of HAS in rats fed rice protein differed considerably from those in rats fed soy protein despite the similar amounts of resistant protein in both sources. More cecal butyrate and less succinate were found in rats fed rice protein and vice versa in rats fed soy protein, suggesting that the quality of resistant protein might be just as important as the quantity in controlling fermentation in rat cecum. The fermentation rate as well as the amino acid composition of resistant protein might be major factors. The importance of the latter has been well documented in ruminants. Salter et al. (1979) found methionine to be a limiting amino acid for rumen bacteria that ferment a low quality roughage diet (low protein diet). Whanger and Matrone (1965 and 1966) also showed in ruminant studies that sulfur plays an essential role for promoting fermentability of complex carbohydrates and SCFA production, particularly n-butyrate, in the rumen. Because sulfur in the rumen and colon is derived mainly from dietary sulfur amino acids and inorganic sulfate, it is likely that an indigestible sulfur amino acid included in resistant protein fraction may also contribute to n-butyrate production in rat cecum. As described previously (Morita et al. 1996 ), among sulfur-amino acids, the methionine content of soy protein was considerably lower (13 g/kg soy protein) than that of rice protein (22 g/kg rice protein). This difference in methionine content might play a role in the differing potency of these proteins in promoting cecal butyrate production in rats.

Our aim in this study was to examine whether it is possible to explain in a consistent manner the role of resistant protein and peptides in controlling cecal fermentation in rats fed rapidly fermentable carbohydrates such as RPS, FOS and HAS. In addition, the relationship between the quality of resistant protein and cecal fermentation was investigated in rats fed resistant starch, with a particular focus on the role of dietary sulfur amino acids on n-butyrate production. For this purpose, oligo-L-methionine (OM), consisting mainly of penta- to undecapeptides, was prepared enzymatically. As previously described (Chiji et al. 1990 , Hara and Kiriyama 1991 , Kasai et al. 1992 ), OM is slowly digested in the small intestine and considerable portions enter the cecum and colon.

	MATERIALS AND METHODS

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS Feeding studies RESULTS DISCUSSION REFERENCES

 
Materials.

Alkaline-extracted rice protein (122.6 mg nitrogen/g) was prepared as described previously (Morita et al. 1996 ). Casein (125.5 mg nitrogen/g) and soybean protein (126.2 mg nitrogen/g) were purchased from New Zealand Dairy Board (Wellington, New Zealand) and Fuji Oil (Osaka, Japan), respectively. The sulfur amino acid concentrations of casein, soy and rice proteins were 29.2, 21.4 and 31.6 g/kg, respectively (Morita et al. 1997 ). The total dietary fiber content of rice and soy proteins was determined by the method of Prosky et al. (1988) to be 11 and 18 g/kg, respectively. The apparent digestibilities of casein, rice and soy proteins were 96, 94 and 93%, respectively, as described previously (Morita et al. 1998 ). High amylose cornstarch (Hi-maize) was purchased from Starch Australasia (Lane Cove, New South Wales, Australia). Raw potato starch (RPS) and fructooligosaccharide (FOS, Meioligo P; purity, >95%) were purchased from Hokuren (Sapporo, Japan) and Meiji Seika (Tokyo, Japan).

Oligo-L-methionine (OM) was synthesized enzymatically from L-methionine ethyl ester sulfate with papain by a previously described method (Jost et al. 1980 ). The preparation obtained was characterized in detail by Kasai et al. (1992) and found to consist of 5–11 mers of oligo-L-methionine.

Care of animals.

Male rats of the Sprague-Dawley strain (purchased from Shizuoka Laboratory Animal Center, Hamamatsu, Japan) were housed in individual stainless steel cages with wire screen bottoms in a room with controlled temperature (23 ± 2°C) and lighting (lights on from 0800 to 2000 h). After adaptation to a casein-cornstarch diet (Table 1 ) for at least 5 d, rats were divided into groups on the basis of body weight and allowed free access to experimental diets and water. Body weight and food intake were recorded each morning before replenishing the diet. None of the diet used in this study contained cellulose or any other source of dietary fiber to avoid any confounding effects on the fermentation products of RPS, FOS and HAS, and interaction with dietary protein.

	Feeding studies

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS Feeding studies RESULTS DISCUSSION REFERENCES

 
Effects of casein, soy and rice proteins on cecal fermentation in rats fed a RPS diet (Experiment 1).

After acclimation, 18 rats weighing 178–188 g were divided into three groups (n = 6) and were allowed free access to diets containing casein, soy or rice protein (250 g/kg diet) for 13 d. The composition of each test diet was the same as that of the casein-cornstarch diet (Table 1) except for the protein and carbohydrate sources. Raw potato starch (200 g/kg diet) was added to each diet at the expense of an equal amount of cornstarch, i.e., the total amount of dietary starch was the same (655 g/kg diet) in all diets. The soy or rice protein was added to each diet at the expense of an equal amount of casein. Feces were collected for the last 3 d of the experimental period, freeze-dried and stored at -20°C. At the end of the experimental period, rats were anesthetized with diethyl ether at 1300–1500 h, and the cecum was removed and weighed. The cecal contents were transferred to a 50-mL screw-capped glass tube and stored at -20°C until analysis. The cecal wall was flushed clean with ice-cold 0.15 mol/L NaCl, gently blotted on filter paper and weighed.

Effects of casein, soy and rice proteins on cecal fermentation in rats fed a FOS diet (Experiment 2).

After acclimation, 18 rats weighing 179–188 g were divided into three groups (n = 6) and were allowed free access to diets containing casein, soy or rice protein (250 g/kg diet) for 13 d. The basic composition of each diet was the same as that of the casein-cornstarch diet (Table 1) except for the protein and carbohydrate sources. Fructooligosaccharide (60 g/kg diet) was added to each diet at the expense of an equal amount of cornstarch. The soy or rice protein was added to each diet at the expense of an equal amount of casein. Fecal collection, sampling of cecal contents and their analyses were as described for Experiment 1.

Apparent digestibility of OM in ileorectostomized rats (Experiment 3).

After acclimation to the casein-cornstarch diet, 18 rats weighing (350–400 g) were subjected to ileorectostomy in which the distal ileum is anastomosed to the rectum as described previously (Nishimura et al. 1993 ). Rats subjected to this operation were not allowed food and water for the first 24 h postoperation; they received daily intramuscular injections of 10 µL of Mycillin Sol [containing procaine penicillin G (200 g/L) and dihydrostreptomycin sulfate (250 g/L); Toyo Jozo, Shizuoka, Japan] on d 0–3 after surgery. They were then fed the casein-cornstarch diet (Table 1) for 10 d. Constant growth rates (5–7 g body weight gain/d) were achieved with this diet after 7 d. After postoperative recovery, rats weighing 354–457 g were divided into three groups (n = 6) on the basis of body weight.

Rats were allowed free access to one of three diets for 7 d. The basic composition of each diet was the same as that of the casein-cornstarch diet (Table 1) . The first group was fed the casein-cornstarch diet, and the remaining two groups were fed the casein-cornstarch diet containing either 5 or 10 g of OM/kg diet. The addition of OM was at the expense of casein. Feces were collected for the last 3 d of the experimental period, freeze-dried and stored at -20°C.

Apparent digestibility of OM was calculated by using the following equation on the premise that an equal amount of methionine derived from casein was excreted into feces in all dietary groups. Determination of fecal methionine was described previously (Morita et al. 1996 ).

Effects of OM supplementation on cecal fermentation in rats fed an HAS diet (Experiment 4).

After acclimation, 30 rats weighing 170–178 g were divided into five groups (n = 6) and were allowed free access to one of the respective diets (casein, OM-supplemented casein, soy protein, OM-supplemented soy protein or rice protein) for 10 d. In this experiment, the basic composition of each diet was the same as that of the casein-cornstarch diet (Table 1) except for the carbohydrate and protein sources and supplementation of OM. High amylose cornstarch (200 g/kg diet) was added to each diet at the expense of an equal amount of cornstarch, i.e., the total amount of dietary starch was the same (655 g/kg diet) in all diets. The soy or rice protein was added to each diet at the expense of an equal amount of casein. Supplementation of OM (3 g/kg) diet was accomplished by replacing an equal weight of cornstarch with OM.

Analytical procedures.

After homogenizing cecal contents, a portion of homogenate was diluted with the same weight of distilled water; cecal pH was then measured with a compact pH meter (Model C-1, Horiba, Tokyo, Japan). Cecal ammonia was determined spectrophotometrically in deproteinized [4 mL of 0.25 mol/L sulfuric acid and 50 g/L sodium tungstate dihydrate (1: 1, v/v), for 50 mg of cecal contents] supernatant (1500 x g, 10 min) of cecal contents (Okuda and Fujii 1966 ). Measurement of cecal organic acids (formate, acetate, propionate, isobutyrate, n-butyrate, isovalerate, n-valerate, citrate, malate, succinate and lactate) was described previously (Morita et al. 1998 ). Fecal starch was determined using a Megazyme Total Starch Assay Kit (Megazyme Australia, Sydney, Australia) with a modification that involved preheating the samples in dimethylsulfoxide at 100°C for 30 min (Muir et al. 1995 ). Fecal nitrogen was measured by the Kjeldahl method (Miller and Houghton 1945 ).

Statistical analyses.

Data were analyzed by ANOVA; significant differences among means were separated by Duncan's multiple range test (Shibata 1974 ) or the Scheffé test (when sample number was different among the groups). When variances were not homogeneous by the Bartlett test (Zar 1984 ), data were logarithmically transformed, and transformed data were analyzed by ANOVA followed by multiple comparison. When variances were not homogenous even after logarithmic transformation, the results were presented as medians with range and then analyzed by Kruskal-Wallis ANOVA followed by the Kolmogorov-Smirnov two-sample test (Zar 1984 ). All statements of significant differences show the 5% level of probability.

	RESULTS

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS Feeding studies RESULTS DISCUSSION REFERENCES

 
Effects of casein, soy and rice proteins on cecal fermentation in rats fed RPS diet (Experiment 1).

There were no significant differences in food intake and body weight gain among the groups (Table 2 ). Cecal tissue weights were significantly greater in rats fed casein than in the other two groups although the weight of cecal contents did not differ among the groups. Cecal pH was lowest in rats fed soy protein, highest in rats fed rice protein and intermediate in rats fed casein. There were no significant differences in cecal ammonia among the groups.

Effects of casein, soy and rice proteins on cecal fermentation in rats fed FOS diet (Experiment 2).

In this experiment, all rats were fed FOS with one of three sources of protein. Although food intake in rats fed casein was significantly lower than that in rats fed soy or rice protein, there were no significant differences in body weight gain among the groups (Table 3 ). The weights of cecal contents were not different among the groups, but the weights of cecal tissue were significantly higher in rats fed casein or soy protein than in those fed rice protein. Cecal pH and ammonia did not differ among the groups.

Apparent digestibility of OM in ileorectostomized rats (Experiment 3).

There were no significant differences in food intake, body weight gain or fecal dry weight among the groups (Table 4 ). Fecal excretions of methionine in rats fed both OM-supplemented casein diets were significantly higher than those in rats fed casein alone. The amount of fecal methionine in the 1.0% OM-supplemented casein group was more than double that of the 0.5% OM-supplemented casein group (P < 0.05). However, apparent digestibilities of OM did not differ between the two groups.

Food intake differed among the groups and was highest in rats fed rice protein, lowest in rats fed casein and intermediate in rats fed the other three diets (Table 5). However, body weight gain did not differ among the groups. The weight of cecal contents did not differ among the groups, but the cecal tissue weights were significantly higher in rats fed casein + 0.3% OM than in rats fed rice protein. The other three groups showed intermediate weights and there were no significant differences among the three groups. Cecal pH was significantly higher in rats fed rice protein than in those fed casein, casein + 0.3% OM and soy protein, but there were no significant differences between the groups fed rice protein and soy protein + 0.3% OM. The OM supplementation to soy protein significantly raised cecal pH compared with soy protein alone. There were no significant differences in cecal ammonia among the groups.

Fecal dry weight was significantly greater in rats fed soy protein, soy protein + 0.3% OM and rice protein than in those fed casein and casein + 0.3% OM. Fecal starch excretion was lowest in rats fed rice protein. The OM supplementation to casein significantly reduced fecal starch compared with casein alone. Although fecal starch excretion in rats fed soy protein + 0.3% OM was also reduced to one half of that in rats fed soy protein alone, the high variance resulted in differences that were not significant. Fecal nitrogen excretion was highest in rats fed rice protein, lowest in rats fed casein and casein + 0.3% OM, and intermediate in the soy protein and soy protein + 0.3% OM groups.

	DISCUSSION

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS Feeding studies RESULTS DISCUSSION REFERENCES

 
Interest in colonic fermentation of butyrate has increased since reports of its antineoplastic effects (Candido et al. 1978 , Kim et al. 1980 , McIntyre et al. 1993 , Whitehead et al. 1986 ) indicate a possible linkage between the fermentation of dietary fiber/resistant starch and the prevention of large bowel cancer. However, apart from SCFA, bacterial fermentation of carbohydrates also produces other organic acids such as lactate, succinate and formate (Cummings and Macfarlane 1991 ), and the type of carbohydrate fermented and dietary condition may affect fermentation products (Englyst et al. 1987 ). Thus, a fermentation strategy favoring SCFA production should be established to elucidate the potentially beneficial effects of SCFA on large bowel physiology.

In this study, the effects of resistant protein and their interactions with RPS, FOS and HAS on large bowel SCFA have been further examined in rats. As expected from earlier studies (Levrat et al. 1991 , Morita et al. 1998 ), we found that consumption of RPS or FOS with casein also resulted in large amounts of cecal succinate and/or lactate, which are normally detected as minor organic acids. In rats fed RPS with casein, the most predominant organic acid was acetate, but lactate as well as succinate was also found in considerable amounts, i.e., the sum of these cecal pool sizes reached 324 µmol (Table 2) . In rats fed FOS with casein, the cecal pool size of succinate equaled or exceeded the sum of SCFA (Table 3) . In contrast, when rice protein was fed instead of casein, the contribution of lactate was much less, whereas that of propionate was higher in rats fed RPS. n-Butyrate also increased substantially (Table 2) . In rats fed rice protein with FOS, cecal pool size of n-butyrate and acetate were significantly greater with profoundly lower levels of succinate (Table 3) . These results in HAS feeding with casein or rice protein were similar to those obtained in FOS feeding (Table 5) and agreed with previous results (Morita et al. 1998 ).

The reason for the greater level of lactate or succinate in rats fed RPS, FOS or HAS with casein is not completely understood. However, findings from the in vitro studies using isolated cultures such as Bacteroides and Clostridium (Macfarlane and Macfarlane 1993 ) suggested that nutritional availability of bacteria could influence fermentation end products, i.e., under nitrogen-limited growth conditions, increased production of electron-sink products such as succinate and lactate occurred, and less SCFA were formed at a high growth rate or during growth in the presence of excess carbohydrate. In contrast, under carbohydrate-limited growth conditions, more SCFA and less succinate or lactate were produced. These in vitro findings as well as the in vivo findings obtained from the present and previous studies (Morita et al. 1998 ) strongly suggest that an imbalance occurs in the ratio of carbohydrate and nitrogen in rats fed large amounts of rapidly fermentable carbohydrates with highly digestible casein as the sole protein source, and this imbalance may induce metabolic change in bacterial fermentation leading to the accumulation of lactate and/or succinate. Therefore, we conclude that resistant protein and peptides promote cecal butyrate production primarily as a result of a change in bacterial metabolism through a correction of the imbalance.

Another explanation for the higher concentrations of cecal lactate and succinate may be pH. When rats were fed graded levels of HAS or RPS with casein, cecal pH decreased with increasing dietary HAS or RPS level and was negatively correlated with cecal succinate or lactate concentration (Ikai and Morita, unpublished observation). Succinate and lactate are normal fermentation products and these organic acids are normally further utilized by other bacteria (Cummings 1981 , Macfarlane and Gibson 1995 ). However, the extremely low cecal pH observed in rats fed RPS or HAS with casein (Tables 2 and 5) may have induced a change in the microflora, resulting in the disappearance of the normally predominant cecal bacteria including lactate- or succinate-utilizing species such as Bacteroides (Caldarini et al. 1996 ). This acidic condition favors acid-tolerant bacteria, leading to a further accumulation of lactate or succinate. Subsequently, the increased lactate or succinate concentration further depressed cecal pH, i.e., a vicious cycle may occur. Cecal pH in rats fed RPS or HAS with rice protein was significantly higher than that in rats fed RPS or HAS with casein, whereas contribution of succinate and/or lactate in rats fed rice protein was much less than in rats fed casein (Tables 2 and 5) . At present, therefore, we think an imbalance of carbohydrate and nitrogen as fermentative substrates may trigger a metabolic change of bacteria followed by an accumulation of succinate and/or lactate; subsequent lowering of the cecal pH by these acids may exacerbate abnormal fermentation through a change in microflora.

Of further interest in the effects of resistant protein is the differing potency of rice and soy proteins on cecal SCFA production. Unlike rice protein, soy protein did not decrease cecal pool size of succinate or lactate in rats fed RPS, FOS or HAS (Tables 2 , 3 and 5) compared with those fed casein. Although soy protein increased cecal pool size of acetate only in rats fed FOS or HAS, that of n-butyrate was unaffected in rats fed RPS, FOS or HAS (Tables 2 , 3 and 5) . Although rice and soy proteins have a similar apparent digestibility (Morita et al. 1996 ), the effects of these proteins on cecal fermentation differed remarkably. Two possibilities exist, i.e., the different rates at which resistant protein becomes available to the bacteria and the different amino acid composition that enters the cecum and colon. In this study, we attempted to clarify the importance of the latter by using a slowly digestible OM with an apparent digestibility of ~30% (Table 4) . In rats fed the HAS diet, OM supplementation to casein doubled the pool size of cecal n-butyrate compared with casein alone, whereas cecal succinate was not affected by OM supplementation (Table 5) . The same tendency was observed when OM was supplemented to soy protein; the pool size of cecal n-butyrate increased significantly and equaled or exceeded that observed in rats fed HAS with rice protein (Table 5) . We also found in rats fed HAS that OM supplementation to casein or soy protein significantly decreased fecal starch excretion compared with that in rats fed casein or soy protein alone (Table 5) , suggesting that OM was effective not only in promoting cecal n-butyrate production but also in improving cecal fermentability of HAS. Salter et al. (1979) showed that providing methionine to rumen bacteria that ferment a low protein diet improved their growth rate and fermentability of complex carbohydrates. Whanger and Matrone (1965 and 1966) also showed that sulfur is essential for rumen bacteria to promote fermentation of complex carbohydrates and bacterial protein synthesis, to produce SCFA, particularly n-butyrate, and to prevent accumulation of lactate in the rumen. Therefore, in examining the role of methionine in bacterial fermentation, it is possible that a similar mechanism may function in rat cecum and calf rumen. The differing potency of rice and soy proteins in promoting large bowel fermentation of HAS is explained in part by the difference in methionine content between soy and rice proteins. The relevance of the fermentation rate of resistant protein remains to be established. Nevertheless, these results may have an implication for human large bowel fermentation. Fermentation products of resistant starch or other indigestible carbohydrate in the large bowel may be considerably affected by food, as previously suggested by Annison and Topping (1994) .

	FOOTNOTES

 
¹ Presented in part at the Annual Meeting of the Japanese Society of Nutrition and Food Science, April 1998, Okinawa, Japan [Morita, T., (1998) Resistant protein controls cecal fermentation. p. 37 (abs.)].

³ Abbreviations used: FOS, fructooligosaccharide; HAS, high amylose cornstarch; OM, oligo-L-methionine; RPS, raw potato starch; SCFA, short-chain fatty acid.

Manuscript received January 4, 1999. Initial review completed February 10, 1999. Revision accepted April 2, 1999.

	REFERENCES

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS Feeding studies RESULTS DISCUSSION REFERENCES

 

1. American Institute of Nutrition Report of the American Institute of Nutrition ad noc committee on standards for nutritional studies. J. Nutr. 1977;107:1340-1348

2. Annison G., Topping D. L. Nutritional role of resistant starch: chemical structure vs physiological function. Annu. Rev. Nutr. 1994;14:297-320[Medline]

3. Caldarini M. I., Pons S., D'agostino D., Depaula J. A., Greco G., Negri G., Ascione A., Bustos D. Abnormal fecal flora in a patient with short bowel syndrome. Dig. Dis. Sci. 1996;41:1649-1652[Medline]

4. Candido E. P., Reeves R., Davies J. R. Sodium butyrate inhibits histone deacetylation in cells. Cell 1978;14:105-114[Medline]

5. Chiji H., Harayama K., Kiriyama S. Effects of feeding rats low protein diets containing casein or soy protein isolate supplemented with methionine or oligo-L-methionine. J. Nutr. 1990;120:166-171

6. Cummings J. H. Short chain fatty acids in the human colon. Gut 1981;22:763-779[Free Full Text]

7. Cummings J. H., Macfarlane G. T. The control and consequences of bacterial fermentation in the human large intestine. J. Appl. Bacteriol. 1991;70:443-459[Medline]

8. Englyst H. N., Hay S., Macfarlane G. T. Polyssacharide breakdown by mixed populations of human faecal bacteria. FEMS Microbiol. Ecol. 1987;95:163-171

9. Hara H., Kiriyama S. Absorptive behavior of oligo-L-methionine and dietary proteins in a casein or soybean protein diet: porto-venous differences in amino acid concentrations in unrestrained rats. J. Nutr. 1991;121:638-645

10. Hidaka H., Eida T., Takizawa T., Tokunaga T., Tashiro Y. Effects of fructo-oligosaccharides on intestinal flora and human health. Bifid. Microflora 1986;5:37-50

11. Hosoya N., Dhorranintra B., Hidaka H. Utilization of [U-¹⁴C] fructo-oligosaccharides in man as energy resources. J. Clin. Biochem. Nutr. 1988;5:67-74

12. Jost R., Brambilla E., Monti J. C., Luisi P. L. Papain catalyzed polymerization of -amino acids. Synthesis and characterization of water insoluble oligomer of L-methionine. Helv. Chim. Acta 1980;63:375-384

13. Kasai T., Tanaka T., Kiriyama S. Correlation between molecular weight distribution of oligo-L-methionine prepared by papain-catalyzed polymerization and its supplementary effect in a low protein diet. Biosci. Biotechnol. Biochem. 1992;56:1884-1885

14. Kim Y. S., Tsao D., Siddiqui B., Whitehead J. S., Arnstein P., Bennet J., Hicks J. Effects of sodium butyrate and dimethylsulfoxide on biochemical properties of human colon cancer cell. Cancer 1980;45:1185-1192[Medline]

15. Levrat M. A., Rémésy C., Demigné C. Very acidic fermentations in the rat cecum during adaptation to a diet rich in amylose-resistant starch (crude potato starch). J. Nutr. Biochem. 1991;2:31-36

16. Macfarlane G. T., Gibson G. R. Microbiological aspects of the production of short-chain fatty acids in the large bowel. Cummings J.H. Rombeau J.L. Sakata T. eds. Physiological and Clinical Aspects of Short-Chain Fatty Acids 1995:87-105 Cambridge University Press Cambridge, UK.

17. Macfarlane G. T., Macfarlane S. Factors affecting fermentation reactions in the large bowel. Proc. Nutr. Soc. 1993;52:367-373[Medline]

18. McIntyre A., Gibson P. R., Young G. P. Butyrate production from dietary fiber and protection against large bowel cancer in a rat model. Gut 1993;34:386-391[Abstract/Free Full Text]

19. Miller L., Houghton J. A. The micro-Kjeldahl determination of the nitrogen content of amino acids and proteins. J. Biol. Chem. 1945;159:373-380[Free Full Text]

20. Morita T., Kasaoka S., Oh-hashi A., Ikai M., Numasaki Y., Kiriyama S. Resistant proteins alter cecal short-chain fatty acid profiles in rats fed high amylose cornstarch. J. Nutr. 1998;128:1156-1164[Abstract/Free Full Text]

21. Morita T., Oh-hashi A., Kasaoka S., Ikai M., Kiriyama S. Rice protein isolates produced by the two different methods lower serum cholesterol concentration in rats compared with casein. J. Sci. Food Agric. 1996;71:415-424

22. Morita T., Oh-hashi A., Takei K., Ikai M., Kasaoka S., Kiriyama S. Cholesterol-lowering effects of soybean, potato, and rice proteins depend on their low methionine contents in rats fed a cholesterol-free purified diet. J. Nutr. 1997;127:470-477[Abstract/Free Full Text]

23. Muir J. G., Birkett A., Brown I., Jones G., O'Dea K. Food processing and maize variety affect amounts of starch escaping digestion in the small intestine. Am. J. Clin. Nutr. 1995;61:82-89[Abstract/Free Full Text]

24. Nishimura N., Nishikawa H., Kiriyama S. Ileorectostomy or cecectomy but not colectomy abolishes the plasma cholesterol-lowering effect of dietary beet fiber in rats. J. Nutr. 1993;123:1260-1269

25. Okuda H., Fujii S. Kettyuu anmonia tyokusetu hishoku teiryouhou. The Saishin-Igaku (in Japanese) 1966;21:622-627

26. Prosky L., Asp N. G., Schweizer T. F., Devries J. W., Furda I. Determination of insoluble, soluble, and total dietary fiber in food and food products: interlaboratory study. J. Assoc. Off. Anal. Chem. 1988;71:1017-1023[Medline]

27. Roediger W. E. W. Role of anaerobic bacteria in the metabolic welfare of the colonic mucosa in man. Gut 1980;21:793-798[Abstract/Free Full Text]

28. Salter D. N., Daneshvar K., Smith R. H. The origin of nitrogen incorporated into compounds in the rumen bacteria of steers given protein- and urea-containing diets. Br. J. Nutr. 1979;41:197-209[Medline]

29. Scheppach W., Fabian C., Sachs M., Kasner H. Effect of starch malabsorption on faecal SCFA excretion in man. Scan. J. Gastroenterol. 1988;23:755-759[Medline]

30. Shibata, K. (1974) In: Basic Statistics for Biologists (in Japanese), pp. 64. Sobun Publishing, Tokyo, Japan.

31. Whanger P. D., Matrone G. Effect of dietary sulfur upon the fatty acid production in the rumen. Biochim. Biophys. Acta 1965;98:454-461[Medline]

32. Whanger P. D., Matrone G. Effect of dietary sulfer upon the production and absorption of lactate in sheep. Biochim. Biophys. Acta 1966;124:273-279[Medline]

33. Whitehead R. H., Young G. P., Bhathal P. S. Effects of short chain fatty acids on a new human colon carcinoma cell line (LM 1215). Gut 1986;27:1457-1463[Abstract/Free Full Text]

34. Zar J. H. Biostatistical Analysis 2nd ed. 1984 Prentice-Hall Englewood Cliffs, NJ.

This article has been cited by other articles:

				R. K. Le Leu, I. L. Brown, Y. Hu, and G. P. Young Effect of resistant starch on genotoxin-induced apoptosis, colonic epithelium, and lumenal contents in rats Carcinogenesis, August 1, 2003; 24(8): 1347 - 1352. [Abstract] [Full Text] [PDF]

				N. M. Delzenne, N. Kok, P. Deloyer, and G. Dandrifosse Dietary Fructans Modulate Polyamine Concentration in the Cecum of Rats J. Nutr., October 1, 2000; 130(10): 2456 - 2460. [Abstract] [Full Text]

				T. Morita, S. Kasaoka, K. Hase, and S. Kiriyama Psyllium Shifts the Fermentation Site of High-Amylose Cornstarch toward the Distal Colon and Increases Fecal Butyrate Concentration in Rats J. Nutr., November 1, 1999; 129(11): 2081 - 2087. [Abstract] [Full Text]

This Article Abstract Full Text (PDF) Purchase Article View Shopping Cart Alert me when this article is cited Alert me if a correction is posted Services Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Morita, T. Articles by Kiriyama, S. Search for Related Content PubMed PubMed Citation Articles by Morita, T. Articles by Kiriyama, S.